Neuregulin-1 protects against neurotoxicities induced by Swedish amyloid precursor protein via the ErbB4 receptor

Neuroscience

Volumn 202, Issue , 2012, Pages 413-423

  Woo, R S ^a   Lee, J H ^a   Kim, H S ^b,c   Baek, C H ^a   Song, D Y ^a   Suh, Y H ^b   Baik, T K ^a  

^a Eulji University   (South Korea)

^b Seoul National University   (South Korea)

^c Seoul National University Bundang Hospital   (South Korea)

Author keywords

Alzheimer's disease; Amyloid beta peptide; ErbB4; Neuregulin1; Swedish mutation of amyloid precursor protein

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; CASPASE 3; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 4; LACTATE DEHYDROGENASE; NEU DIFFERENTIATION FACTOR; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOACCUMULATION; BRAIN NERVE CELL; CELL SURVIVAL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; EMBRYO; ENZYME ACTIVATION; ENZYME RELEASE; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; MITOCHONDRIAL MEMBRANE POTENTIAL; MUTAGENESIS; NERVE CELL NECROSIS; NEUROPROTECTION; NEUROTOXICITY; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; UPREGULATION;

AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CASPASE 3; CELL DEATH; CELLS, CULTURED; DNA; IMMUNOPRECIPITATION; IN SITU NICK-END LABELING; L-LACTATE DEHYDROGENASE; MEMBRANE POTENTIALS; MITOCHONDRIAL MEMBRANES; NEUREGULIN-1; NEURONS; NEUROPROTECTIVE AGENTS; PEPTIDE FRAGMENTS; PLASMIDS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RECEPTOR, EPIDERMAL GROWTH FACTOR; TRANSFECTION;

EID: 84856231939     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.11.026     Document Type: Article

References (57)

1. Anton E.S., Marchionni M.A., Lee K.F., Rakic P. Role of GGF/neuregulin signaling in interactions between migrating neurons and radial glia in the developing cerebral cortex. Development 1997, 124:3501-3510.
2. Bueler H. Mitochondrial dynamics, cell death and the pathogenesis of Parkinson's disease. Apoptosis 2010, 15:1336-1353.
3. Buonanno A., Fischbach G.D. Neuregulin and ErbB receptor signaling pathways in the nervous system. Curr Opin Neurobiol 2001, 11:287-296.
4. Calaora V., Rogister B., Bismuth K., Murray K., Brandt H., Leprince P., Marchionni M., Dubois-Dalcq M. Neuregulin signaling regulates neural precursor growth and the generation of oligodendrocytes in vitro. J Neurosci 2001, 21:4740-4751.
5. Chen M.S., Bermingham-McDonogh O., Danehy F.T., Nolan C., Scherer S.S., Lucas J., Gwynne D., Marchionni M.A. Expression of multiple neuregulin transcripts in postnatal rat brains. J Comp Neurol 1994, 349:389-400.
6. Citri A., Yarden Y. EGF-ERBB signalling: towards the systems level. Nat Rev Mol Cell Biol 2006, 7:505-516.
7. Clementi M.E., Pezzotti M., Orsini F., Sampaolese B., Mezzogori D., Grassi C., Giardina B., Misiti F. Alzheimer's amyloid beta-peptide (1-42) induces cell death in human neuroblastoma via bax/bcl-2 ratio increase: an intriguing role for methionine 35. Biochem Biophys Res Commun 2006, 342:206-213.
8. Corfas G., Roy K., Buxbaum J.D. Neuregulin 1-erbB signaling and the molecular/cellular basis of schizophrenia. Nat Neurosci 2004, 7:575-580.
9. Croslan D.R., Schoell M.C., Ford G.D., Pulliam J.V., Gates A., Clement C.M., Harris A.E., Ford B.D. Neuroprotective effects of neuregulin-1 on B35 neuronal cells following ischemia. Brain Res 2008, 1210:39-47.
10. Culmsee C., Landshamer S. Molecular insights into mechanisms of the cell death program: role in the progression of neurodegenerative disorders. Curr Alzheimer Res 2006, 3:269-283.
11. Di Segni A., Shaharabani E., Stein R., Pinkas-Kramarski R. Neuregulins rescue PC12-ErbB-4 cells from cell death induced by beta-amyloid peptide: involvement of PI3K and PKC. J Mol Neurosci 2005, 26:57-69.
12. Eckert A., Schindowski K., Leutner S., Luckhaus C., Touchet N., Czech C., Müller W.E. Alzheimer's disease-like alterations in peripheral cells from presenilin-1 transgenic mice. Neurobiol Dis 2001, 8:331-342.
13. Fernandez P.A., Tang D.G., Cheng L., Prochiantz A., Mudge A.W., Raff M.C. Evidence that axon-derived neuregulin promotes oligodendrocyte survival in the developing rat optic nerve. Neuron 2000, 28:81-90.
14. Fukazawa R., Miller T.A., Kuramochi Y., Frantz S., Kim Y.D., Marchionni M.A., Kelly R.A., Sawyer D.B. Neuregulin-1 protects ventricular myocytes from anthracycline-induced apoptosis via erbB4-dependent activation of PI3-kinase/Akt. J Mol Cell Cardiol 2003, 35:1473-1479.
15. Garcia R.A., Vasudevan K., Buonanno A. The neuregulin receptor ErbB-4 interacts with PDZ-containing proteins at neuronal synapses. Proc Natl Acad Sci U S A 2000, 97:3596-3601.
16. Gerecke K.M., Wyss J.M., Carroll S.L. Neuregulin-1beta induces neurite extension and arborization in cultured hippocampal neurons. Mol Cell Neurosci 2004, 27:379-393.
17. Gerecke K.M., Wyss J.M., Karavanova I., Buonanno A., Carroll S.L. ErbB transmembrane tyrosine kinase receptors are differentially expressed throughout the adult rat central nervous system. J Comp Neurol 2001, 433:86-100.
18. Goldshmit Y., Erlich S., Pinkas-Kramarski R. Neuregulin rescues PC12-ErbB4 cells from cell death induced by H(2)O(2). Regulation of reactive oxygen species levels by phosphatidylinositol 3-kinase. J Biol Chem 2001, 276:46379-46385.
19. Guo W.P., Fu X.G., Jiang S.M., Wu J.Z. Neuregulin-1 regulates the expression of Akt, Bcl-2, and Bad signaling after focal cerebral ischemia in rats. Biochem Cell Biol 2010, 88:649-654.
20. Hanson A.J., Prasad J.E., Nahreini P., Andreatta C., Kumar B., Yan X.D., Prasad K.N. Overexpression of amyloid precursor protein is associated with degeneration, decreased viability, and increased damage caused by neurotoxins (prostaglandins A1 and E2, hydrogen peroxide, and nitric oxide) in differentiated neuroblastoma cells. J Neurosci Res 2003, 74:148-159.
21. Holmes W.E., Sliwkowski M.X., Akita R.W., Henzel W.J., Lee J., Park J.W., Yansura D., Abadi N., Raab H., Lewis G.D., et al. Identification of heregulin, a specific activator of p185erbB2. Science 1992, 256:1205-1210.
22. Hu X., Hicks C.W., He W., Wong P., Macklin W.B., Trapp B.D., Yan R. Bace1 modulates myelination in the central and peripheral nervous system. Nat Neurosci 2006, 9:1520-1525.
23. Huang Y.Z., Won S., Ali D.W., Wang Q., Tanowitz M., Du Q.S., Pelkey K.A., Yang D.J., Xiong W.C., Salter M.W., Mei L. Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses. Neuron 2000, 26:443-455.
24. Joo Y., Kim H.S., Woo R.S., Park C.H., Shin K.Y., Lee J.P., Chang K.A., Kim S., Suh Y.H. Mefenamic acid shows neuroprotective effects and improves cognitive impairment in in vitro and in vivo Alzheimer's disease models. Mol Pharmacol 2006, 69:76-84.
25. Kang J., Lemaire H.G., Unterbeck A., Salbaum J.M., Masters C.L., Grzeschik K.H., Multhaup G., Beyreuther K., Müller-Hill B. The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 1987, 325:733-736.
26. Lai C., Lemke G. An extended family of protein-tyrosine kinase genes differentially expressed in the vertebrate nervous system. Neuron 1991, 6:691-704.
27. Lautraite S., Bigot-Lasserre D., Bars R., Carmichael N. Optimisation of cell-based assays for medium throughput screening of oxidative stress. Toxicol In Vitro 2003, 17:207-220.
28. Law A.J., Shannon Weickert C., Hyde T.M., Kleinman J.E., Harrison P.J. Neuregulin-1 (NRG-1) mRNA and protein in the adult human brain. Neuroscience 2004, 127:125-136.
29. Lee H.J., Jung K.M., Huang Y.Z., Bennett L.B., Lee J.S., Mei L., Kim T.W. Presenilin-dependent gamma-secretase-like intramembrane cleavage of ErbB4. J Biol Chem 2002, 277:6318-6323.
30. Lesne S., Koh M.T., Kotilinek L., Kayed R., Glabe C.G., Yang A., Gallagher M., Ashe K.H. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 2006, 440:352-357.
31. Li B., Woo R.S., Mei L., Malinow R. The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity. Neuron 2007, 54:583-597.
32. Li B.S., Ma W., Jaffe H., Zheng Y., Takahashi S., Zhang L., Kulkarni A.B., Pant H.C. Cyclin-dependent kinase-5 is involved in neuregulin-dependent activation of phosphatidylinositol 3-kinase and Akt activity mediating neuronal survival. J Biol Chem 2003, 278:35702-35709.
33. Li Y., Xu Z., Ford G.D., Croslan D.R., Cairobe T., Li Z., Ford B.D. Neuroprotection by neuregulin-1 in a rat model of permanent focal cerebral ischemia. Brain Res 2007, 1184:277-283.
34. Liu Y., Ford B., Mann M.A., Fischbach G.D. Neuregulins increase alpha7 nicotinic acetylcholine receptors and enhance excitatory synaptic transmission in GABAergic interneurons of the hippocampus. J Neurosci 2001, 21:5660-5669.
35. Lopez-Bendito G., Cautinat A., Sánchez J.A., Bielle F., Flames N., Garratt A.N., Talmage D.A., Role L.W., Charnay P., Marín O., Garel S. Tangential neuronal migration controls axon guidance: a role for neuregulin-1 in thalamocortical axon navigation. Cell 2006, 125:127-142.
36. Lukiw W.J., Bazan N.G. Survival signaling in Alzheimer's disease. Biochem Soc Trans 2006, 34:1277-1282.
37. Mattson M.P. Pathways towards and away from Alzheimer's disease. Nature 2004, 430:631-639.
38. Mattson M.P., Meffert M.K. Roles for NF-kappaB in nerve cell survival, plasticity, and disease. Cell Death Differ 2006, 13:852-860.
39. Mei L., Xiong W.C. Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci 2008, 9:437-452.
40. Ni C.Y., Murphy M.P., Golde T.E., Carpenter G. gamma -Secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 2001, 294:2179-2181.
41. Okada M., Corfas G. Neuregulin1 downregulates postsynaptic GABAA receptors at the hippocampal inhibitory synapse. Hippocampus 2004, 14:337-344.
42. Petronilli V., Cola C., Bernardi P. Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore. II. The minimal requirements for pore induction underscore a key role for transmembrane electrical potential, matrix pH, and matrix Ca2+. J Biol Chem 1993, 268:1011-1016.
43. Ricart K., Pearson R., Viera L., Cassina P., Kamaid A., Carroll S.L., Estevez A.G. Interactions between beta-neuregulin and neurotrophins in motor neuron apoptosis. J Neurochem 2006, 97:222-233. J.
44. Rio C., Rieff H.I., Qi P., Khurana T.S., Corfas G. Neuregulin and erbB receptors play a critical role in neuronal migration. Neuron 1997, 19:39-50.
45. Rovelet-Lecrux A., Hannequin D., Raux G., Le Meur N., Laquerrière A., Vital A., Dumanchin C., Feuillette S., Brice A., Vercelletto M., Dubas F., Frebourg T., Campion D. APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy. Nat Genet 2006, 38:24-26.
46. Savonenko A.V., Melnikova T., Laird F.M., Stewart K.A., Price D.L., Wong P.C. Alteration of BACE1-dependent NRG1/ErbB4 signaling and schizophrenia-like phenotypes in BACE1-null mice. Proc Natl Acad Sci U S A 2008, 105:5585-5590.
47. Selkoe D.J. Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 2001, 81:741-766.
48. Selkoe D.J. Deciphering the genesis and fate of amyloid beta-protein yields novel therapies for Alzheimer disease. J Clin Invest 2002, 110:1375-1381.
49. Shyu W.C., Lin S.Z., Chiang M.F., Yang H.I., Thajeb P., Li H. Neuregulin-1 reduces ischemia-induced brain damage in rats. Neurobiol Aging 2004, 25:935-944.
50. Stankovic K., Rio C., Xia A., Sugawara M., Adams J.C., Liberman M.C., Corfas G. Survival of adult spiral ganglion neurons requires erbB receptor signaling in the inner ear. J Neurosci 2004, 24:8651-8661.
51. Steiner H., Blum M., Kitai S.T., Fedi P. Differential expression of ErbB3 and ErbB4 neuregulin receptors in dopamine neurons and forebrain areas of the adult rat. Exp Neurol 1999, 159:494-503.
52. Suh Y.H., Checler F. Amyloid precursor protein, presenilins, and alpha-synuclein: molecular pathogenesis and pharmacological applications in Alzheimer's disease. Pharmacol Rev 2002, 54:469-525.
53. Tanzi R., Gaston S., Bush A., Romano D., Pettingell W., Peppercorn J., Paradis M., Gurubhagavatula S., Jenkins B., Wasco W. Genetic heterogeneity of gene defects responsible for familial Alzheimer disease. Genetica 1993, 91:255-263.
54. Willem M., Garratt A.N., Novak B., Citron M., Kaufmann S., Rittger A., DeStrooper B., Saftig P., Birchmeier C., Haass C. Control of peripheral nerve myelination by the beta-secretase BACE1. Science 2006, 314:664-666.
55. Woo R.S., Li X.M., Tao Y., Carpenter-Hyland E., Huang Y.Z., Weber J., Neiswender H., Dong X.P., Wu J., Gassmann M., Lai C., Xiong W.C., Gao T.M., Mei L. Neuregulin-1 enhances depolarization-induced GABA release. Neuron 2007, 54:599-610.
56. Zhang L., Fletcher-Turner A., Marchionni M.A., Apparsundaram S., Lundgren K.H., Yurek D.M., Seroogy K.B. Neurotrophic and neuroprotective effects of the neuregulin glial growth factor-2 on dopaminergic neurons in rat primary midbrain cultures. J Neurochem 2004, 91:1358-1368.
57. Zhu J., Cole F., Woo-Rasberry V., Fang X.R., Chiang T.M. Type I and type III collagen-platelet interaction: inhibition by type specific receptor peptides. Thromb Res 2007, 119:111-119.